Abstract
Black band disease (BBD) of corals is a complex polymicrobial disease considered to be a threat to coral reef health, as it can lead to mortality of massive reef-building corals. The BBD community is dominated by gliding, filamentous cyanobacteria with a highly diverse population of heterotrophic bacteria. Microbial interactions such as quorum sensing (QS) and antimicrobial production may be involved in BBD disease pathogenesis. In this study, BBD (whole community) samples, as well as 199 bacterial isolates from BBD, the surface mucopolysaccharide layer (SML) of apparently healthy corals, and SML of apparently healthy areas of BBD-infected corals were screened for the production of acyl homoserine lactones (AHLs) and for autoinducer-2 (AI-2) activity using three bacterial reporter strains. AHLs were detected in all BBD (intact community) samples tested and in cultures of 5.5% of BBD bacterial isolates. Over half of a subset (153) of the isolates were positive for AI-2 activity. AHL-producing isolates were further analyzed using LC-MS/MS to determine AHL chemical structure and the concentration of (S)-4,5-dihydroxy-2,3-pentanedione (DPD), the biosynthetic precursor of AI-2. C6-HSL was the most common AHL variant detected, followed by 3OC4-HSL. In addition to QS assays, 342 growth challenges were conducted among a subset of the isolates, with 27% of isolates eliciting growth inhibition and 2% growth stimulation. 24% of BBD isolates elicited growth inhibition as compared to 26% and 32% of the bacteria from the two SML sources. With one exception, only isolates that exhibited AI-2 activity or produced DPD inhibited growth of test strains. These findings demonstrate for the first time that AHLs are present in an active coral disease. It is possible that AI-2 production among BBD and coral SML bacteria may structure the microbial communities of both a polymicrobial infection and the healthy coral microbiome.
Publication types
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Research Support, Non-U.S. Gov't
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Research Support, U.S. Gov't, Non-P.H.S.
MeSH terms
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Acyl-Butyrolactones / isolation & purification
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Acyl-Butyrolactones / metabolism*
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Acyl-Butyrolactones / pharmacology
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Agrobacterium tumefaciens / drug effects
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Agrobacterium tumefaciens / growth & development
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Animals
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Anthozoa / microbiology*
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Chromobacterium / drug effects
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Chromobacterium / growth & development
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Coral Reefs
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Cyanobacteria / metabolism*
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Cyanobacteria / pathogenicity
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Homoserine / analogs & derivatives*
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Homoserine / biosynthesis
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Homoserine / isolation & purification
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Homoserine / pharmacology
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Lactones / isolation & purification
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Lactones / pharmacology
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Microbial Consortia / physiology
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Microbial Interactions
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Pentanes / isolation & purification
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Pentanes / metabolism
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Pentanes / pharmacology
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Polysaccharides, Bacterial / biosynthesis
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Polysaccharides, Bacterial / isolation & purification
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Polysaccharides, Bacterial / pharmacology
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Quorum Sensing*
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Vibrio / drug effects
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Vibrio / growth & development
Substances
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4,5-dihydroxy-2,3-pentanedione
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Acyl-Butyrolactones
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Lactones
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N-octanoylhomoserine lactone
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Pentanes
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Polysaccharides, Bacterial
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Homoserine
Grants and funding
This research was supported by the NSF (grant no. OCE-1208784 to LLR and SRC and OCE-1061352 to SRC) and by Florida International University. The websites are
www.nsf.gov and
www.fiu.edu. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. First author Beth Zimmer is employed by the commercial company Atkins North America. Atkins North America provided support in the form of salary for author BZ, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific role of this author is articulated in the ‘author contributions’ section. Publication of this article was funded in part by Florida International University and in part by the University of Tennessee, Knoxville, Open Access Publishing Funds.